Modulation of the Somatosensory Evoked Potential by Attention and Spinal Cord Stimulation

Introduction: Spinal Cord Stimulation (SCS) is a last-resort treatment for patients with intractable chronic pain in whom pharmacological and other treatments have failed. Conventional tonic SCS is accompanied by tingling sensations. More recent stimulation protocols like burst SCS are not sensed by the patient while providing similar levels of pain relief. It has been previously reported that conventional tonic SCS can attenuate sensory-discriminative processing in several brain areas, but that burst SCS might have additional effects on the medial, motivational-affective pain system. In this explorative study we assessed the influence of attention on the somatosensory evoked brain responses under conventional tonic SCS as well as burst SCS regime. Methods: Twelve chronic pain patients with an implanted SCS device had 2-weeks evaluation periods with three different SCS settings (conventional tonic SCS, burst SCS, and sham SCS). At the end of each period, an electro-encephalography (EEG) measurement was done, at which patients received transcutaneous electrical pulses at the tibial nerve to induce somatosensory evoked potentials (SEP). SEP data was acquired while patients were attending the applied pulses and while they were mind wandering. The effects of attention as well as SCS regimes on the SEP were analyzed by comparing amplitudes of early and late latencies at the vertex as well as brain activity at full cortical maps. Results: Pain relief obtained by the various SCS settings varied largely among patients. Early SEP responses were not significantly affected by attention nor SCS settings (i.e., burst, tonic, and sham). However, late SEP responses (P300) were reduced with tonic and burst SCS: conventional tonic SCS reduced P300 brain activity in the unattended condition, while burst SCS reduced P300 brain activity in both attended and unattended conditions. Conclusion: Burst spinal cord stimulation for the treatment of chronic pain seems to reduce cortical attention that is or can be directed to somatosensory stimuli to a larger extent than conventional spinal cord stimulation treatment. This is a first step in understanding why in selected chronic pain patients burst SCS is more effective than tonic SCS and how neuroimaging could assist in personalizing SCS treatment.

[1]  S. Raja,et al.  Supraspinal Mechanisms of Spinal Cord Stimulation for Modulation of Pain: Five Decades of Research and Prospects for the Future , 2019, Anesthesiology.

[2]  Richard M. Leahy,et al.  MEG/EEG Group Analysis With Brainstorm , 2019, Front. Neurosci..

[3]  Massimiliano Valeriani,et al.  Neurophysiological Comparison Among Tonic, High Frequency, and Burst Spinal Cord Stimulation: Novel Insights Into Spinal and Brain Mechanisms of Action , 2018, Neuromodulation : journal of the International Neuromodulation Society.

[4]  T. Bekinschtein,et al.  Altered neurocognitive processing of tactile stimuli in patients with Complex Regional Pain Syndrome (CRPS) , 2017, bioRxiv.

[5]  A. Mouraux,et al.  Attention to pain! A neurocognitive perspective on attentional modulation of pain in neuroimaging studies , 2017, Cortex.

[6]  M. Tjepkema-Cloostermans,et al.  Effect of Burst Stimulation Evaluated in Patients Familiar With Spinal Cord Stimulation , 2016, Neuromodulation : journal of the International Neuromodulation Society.

[7]  P. Furlong,et al.  Brain activity modifications following spinal cord stimulation for chronic neuropathic pain: A systematic review , 2016, European journal of pain.

[8]  M. Buonocore,et al.  Inhibition of Somatosensory Evoked Potentials During Different Modalities of Spinal Cord Stimulation: A Case Report , 2016, Neuromodulation : journal of the International Neuromodulation Society.

[9]  D. De Ridder,et al.  Burst and Tonic Spinal Cord Stimulation: Different and Common Brain Mechanisms , 2016, Neuromodulation : journal of the International Neuromodulation Society.

[10]  M. Plazier,et al.  Mimicking the brain: evaluation of St Jude Medical’s Prodigy Chronic Pain System with Burst Technology , 2015, Expert review of medical devices.

[11]  François Mauguière,et al.  Processing of nociceptive input from posterior to anterior insula in humans , 2014, Human brain mapping.

[12]  Warren M. Grill,et al.  Mechanisms and models of spinal cord stimulation for the treatment of neuropathic pain , 2014, Brain Research.

[13]  D. Ridder,et al.  Burst Spinal Cord Stimulation Evaluated in Patients With Failed Back Surgery Syndrome and Painful Diabetic Neuropathy , 2014, Neuromodulation : journal of the International Neuromodulation Society.

[14]  Carina Graversen,et al.  Electroencephalography and analgesics , 2014, British journal of clinical pharmacology.

[15]  Sven Vanneste,et al.  Burst spinal cord stimulation for limb and back pain. , 2013, World neurosurgery.

[16]  E. Buchser,et al.  Analgesic Efficacy of High‐Frequency Spinal Cord Stimulation: A Randomized Double‐Blind Placebo‐Controlled Study , 2013, Neuromodulation : journal of the International Neuromodulation Society.

[17]  M. Gierthmuehlen,et al.  Spinal cord stimulation inhibits cortical somatosensory evoked potentials significantly stronger than transcutaneous electrical nerve stimulation. , 2013, Pain physician.

[18]  R. Peeters,et al.  Spinal cord stimulation modulates cerebral function: an fMRI study , 2012, Neuroradiology.

[19]  M. Buonocore,et al.  Inhibition of somatosensory evoked potentials during spinal cord stimulation and its possible role in the comprehension of antalgic mechanisms of neurostimulation for neuropathic pain. , 2012, Minerva anestesiologica.

[20]  C. Graversen,et al.  Randomised clinical trial: pregabalin attenuates experimental visceral pain through sub‐cortical mechanisms in patients with painful chronic pancreatitis , 2011, Alimentary pharmacology & therapeutics.

[21]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

[22]  Théodore Papadopoulo,et al.  Forward Field Computation with OpenMEEG , 2011, Comput. Intell. Neurosci..

[23]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[24]  T. Menovsky,et al.  Burst Spinal Cord Stimulation: Toward Paresthesia‐Free Pain Suppression , 2010, Neurosurgery.

[25]  Bengt Linderoth,et al.  Cholinergic mechanisms involved in the pain relieving effect of spinal cord stimulation in a model of neuropathy , 2008, PAIN.

[26]  J. Polich Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

[27]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[28]  A. Stancák,et al.  Effects of spinal cord stimulation on the cortical somatosensory evoked potentials in failed back surgery syndrome patients , 2007, Clinical Neurophysiology.

[29]  J. Holsheimer,et al.  Effects of Electrode Positioning on Perception Threshold and Paresthesia Coverage in Spinal Cord Stimulation , 2007, Neuromodulation : journal of the International Neuromodulation Society.

[30]  Urs Ribary,et al.  Thalamocortical dysrhythmia syndrome: MEG imaging of neuropathic pain , 2005 .

[31]  T. Papadopoulo,et al.  A common formalism for the Integral formulations of the forward EEG problem , 2005, IEEE Transactions on Medical Imaging.

[32]  M. Frot,et al.  Brain generators of laser-evoked potentials: from dipoles to functional significance , 2003, Neurophysiologie Clinique/Clinical Neurophysiology.

[33]  J. Holsheimer Which Neuronal Elements are Activated Directly by Spinal Cord Stimulation , 2002, Neuromodulation : journal of the International Neuromodulation Society.

[34]  Alan C. Evans,et al.  Enhancement of MR Images Using Registration for Signal Averaging , 1998, Journal of Computer Assisted Tomography.

[35]  R. Treede,et al.  Median and tibial nerve somatosensory evoked potentials: middle-latency components from the vicinity of the secondary somatosensory cortex in humans. , 1997, Electroencephalography and clinical neurophysiology.

[36]  Bengt Linderoth,et al.  Effects of spinal cord stimulation on touch-evoked allodynia involve GABAergic mechanisms. An experimental study in the mononeuropathic rat , 1996, PAIN®.

[37]  R. Kakigi,et al.  Pain-related somatosensory evoked magnetic fields. , 1995, Electroencephalography and clinical neurophysiology.

[38]  R Kakigi,et al.  Topography of somatosensory evoked magnetic fields following posterior tibial nerve stimulation. , 1995, Electroencephalography and clinical neurophysiology.

[39]  R. Seymour,et al.  Effects of peripherally and centrally acting analgesics on somato-sensory evoked potentials. , 1995, British journal of clinical pharmacology.

[40]  S. Palmisani,et al.  High‐Frequency Spinal Cord Stimulation for the Treatment of Chronic Back Pain Patients: Results of a Prospective Multicenter European Clinical Study , 2013, Neuromodulation : journal of the International Neuromodulation Society.

[41]  T. Wolter,et al.  Continuous Versus Intermittent Spinal Cord Stimulation: An Analysis of Factors Influencing Clinical Efficacy , 2012, Neuromodulation : journal of the International Neuromodulation Society.

[42]  Maarten J. IJzerman,et al.  Altered cortical somatosensory processing in chronic stroke: A relationship with post-stroke shoulder pain. , 2011, NeuroRehabilitation.

[43]  M. Peters,et al.  Responses to Median and Tibial Nerve Stimulation in Patients with Chronic Neuropathic Pain , 2004, Brain Topography.

[44]  R D Pascual-Marqui,et al.  Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. , 2002, Methods and findings in experimental and clinical pharmacology.